Applying error management theory to understand the evolution of decision-making in plant defense

尽管植物以被动而闻名，但它们和动物一样，已经进化出了一种非凡的能力，能够感知和应对环境中的威胁信息。然而，与动物不同的是，我们不知道植物是如何优先考虑不同的信息，并评估风险，以“做出”如何应对的决定。本研究项目将使用错误管理理论来评估高黄花植物（Solidago altissima）如何通过从环境中接收到的线索来评估草食性威胁。我们已经知道，在食草动物到来之前，高大的菊科植物可以感知和响应两种不同的空气信号来启动防御：(1)来自主要食草动物物种的吸引配偶的化学物质（信息素）；(2)来自邻近的高大菊科植物受到多面手昆虫攻击时释放的挥发性化学物质。温室和田间实验将进行，以确定线索阈值，哪些基因被不同的线索触发，以及当线索与所受到的损害类型匹配或不匹配时做出反应的成本和收益。最终，由于不做出反应而犯错误的代价将通过由于食草动物的伤害而减少的生殖产出来衡量。结果将揭示高菊是否采取下注对冲方法，并分配防御，以最大限度地减少代价高昂的错误，而不是代价较低的错误。通过从这个新的角度探索植物防御，本研究将大大拓宽我们对植物如何做出决定的理解，并为植物防御食草动物的进化提供见解。植物和食草动物之间的相互作用是陆地生态系统的支柱，因此了解植物如何“决定”保护自己具有从作物保护到控制入侵物种的应用。该项目将支持学生和博士后研究员的培训和指导，并通过宾夕法尼亚州立大学的既定项目开展公共宣传活动。一枝黄花（Solidago altissima）是已知的少数几种能够根据两种挥发性化学信号检测并改变其防御机制的植物之一：一种来自邻近植物，另一种来自关键的专业食草动物的交配活动。温室和田间试验将检验错误管理理论，以阐明在暴露与主要食草动物伤害匹配或不匹配的线索后，高斑棘基因型防御策略的成本和收益。随后对这些实验中植物组织的激素和转录组学分析将确定暴露于线索和昆虫损伤后基因型防御反应的关键机制。在不同的实验场景下，基因型对食草动物的防御反应的有效性将揭示进化选择的压力，这种压力鼓励植物尽量减少对假警报或不会造成严重损害的昆虫的反应，而优先考虑对更具破坏性的敌人的反应。该项目的研究将为了解植物防御如何演变为应对多种威胁提供关键见解，并具有重要的潜力，为开发新的管理策略提供信息，同时提供一个有趣的话题，帮助中学生和高中生以及公众了解常见植物和昆虫物种之间化学通讯的新颖性和重要性。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

Despite their reputation for passivity, plants, like animals, have evolved a remarkable capacity to perceive and respond to information about threats in their environment. Unlike animals, however, it is unknown how plants prioritize different information and assess risk to 'make decisions' about how to respond. This research project will use error management theory to evaluate how tall goldenrod plants (Solidago altissima) assess threats of herbivory from cues that they receive from the environment. It is already known that tall goldenrod can perceive and respond to two different airborne cues to initiate defenses before herbivores arrive: (1) a mate-attracting chemical (pheromone) from a key damaging herbivore species and (2) volatile chemicals released from neighboring tall goldenrod plants that are being attacked by generalist insects. Greenhouse and field experiments will be conducted to determine cue thresholds, what genes are triggered by different cues, and the costs and benefits of responding when cues are matched versus mismatched with the type of damage received. Ultimately the cost of making an error in not responding will be measured by reduced reproductive output due to herbivore damage. The results will reveal whether tall goldenrod takes a bet-hedging approach and allocates defenses to minimize costly errors in favor of less costly errors. By exploring plant defenses from this novel perspective, this research will significantly broaden our understanding of how plants make decisions and provide insight on the evolution of plant defenses against herbivores. Interactions between plants and herbivores are the backbone of terrestrial ecosystems, so understanding how plants 'decide' to defend themselves has applications from crop protection to control of invasive species. The project will support training and mentorship of students and a postdoctoral researcher, as well as public outreach initiatives through established programs at The Pennsylvania State University.Solidago altissima is among the few plant species known to detect and alter its defenses in response to two volatile chemical cues: one from neighboring plants, one from the mating activity of a key, specialist herbivore. Greenhouse and field experiments will test error management theory to elucidate costs and benefits of the defensive strategies of genotypes of S. altissima following exposure to cues that are matched and mismatched with key herbivore damage. Subsequent phytohormone and transcriptomic analyses of plant tissue from these experiments will identify key mechanisms underlying defense responses of the genotypes following exposure to cues and insect damage. Under the various experimental scenarios, the effectiveness of defense responses of the genotypes against herbivores will reveal evolutionary selection pressures that have encouraged plants to minimize responses to false alarms or insects that do not do substantial damage that would reduce fitness, while prioritizing responses against more damaging foes. The research from this project will provide key insight into how plant defenses evolved to handle multiple threats and has significant potential to inform development of novel management tactics while providing an intriguing topic that will help engage middle- and high-school students and the general public in the novelty and significance of chemical communication between common plant and insect species.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.